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Figure 1.  Effects of Sterilization on Overall Filtration Efficiency and Pressure Drop
Effects of Sterilization on Overall Filtration Efficiency and Pressure Drop

Error bars indicate SD; iwg, inches of water gauge; and H2O2, hydrogen peroxide.

Figure 2.  Effects of Sterilization on Filtration Efficiency by Aerosol Size
Effects of Sterilization on Filtration Efficiency by Aerosol Size

Error bars indicate SD; and H2O2, hydrogen peroxide.

1.
Wu  HL, Huang  J, Zhang  CJP, He  Z, Ming  WK.  Facemask shortage and the novel coronavirus disease (COVID-19) outbreak: reflections on public health measures.   EClinicalMedicine. April 3, 2020;100329. doi:10.1016/j.eclinm.2020.100329PubMedGoogle Scholar
2.
Feng  S, Shen  C, Xia  N, Song  W, Fan  M, Cowling  BJ.  Rational use of face masks in the COVID-19 pandemic.   Lancet Respir Med. 2020;8(5):434-436. doi:10.1016/S2213-2600(20)30134-XPubMedGoogle ScholarCrossref
3.
Centers for Disease Control and Prevention. Recommended guidance for extended use and limited reuse of N95 filtering facepiece respirators in healthcare settings. Accessed May 21, 2020. https://www.cdc.gov/niosh/topics/hcwcontrols/recommendedguidanceextuse.html
4.
Viscusi  DJ, Bergman  MS, Eimer  BC, Shaffer  RE.  Evaluation of five decontamination methods for filtering facepiece respirators.   Ann Occup Hyg. 2009;53(8):815-827.PubMedGoogle Scholar
5.
Derrick  JL, Gomersall  CD.  Protecting healthcare staff from severe acute respiratory syndrome: filtration capacity of multiple surgical masks.   J Hosp Infect. 2005;59(4):365-368. doi:10.1016/j.jhin.2004.10.013PubMedGoogle ScholarCrossref
6.
Radonovich  LJ  Jr, Simberkoff  MS, Bessesen  MT,  et al; ResPECT investigators.  N95 respirators vs medical masks for preventing influenza among health care personnel: a randomized clinical trial.   JAMA. 2019;322(9):824-833. doi:10.1001/jama.2019.11645PubMedGoogle ScholarCrossref
5 Comments for this article
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Clarifications
Sumner Barenberg, Ph.D. | Northeastern University
Can the authors clarify the following:
• Define the source and how the plasma vapor hydrogen peroxide was generated
• Define the source, the chemistry and how the gaseous chlorine dioxide was generated
• Define the ppm hrs concentration of each the vapor hydrogen peroxide and gaseous chlorine dioxide used in this study
• Define the exact materials of construction structure of each of the N95, KN95, and surgical masks used in this study with respect hydrophobicity, hydrophilicity, and electrostatic charge
• Cai and Floyd in their article reference a 2009 paper by Viscusi which clearly states that they examined five potential decontamination chemistries.
Of specific interest was that they used bleach not gaseous chlorine dioxide in their paper which generated 6% chlorine gas.
CONFLICT OF INTEREST: None Reported
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To readers
Changjie Cai, Ph.D. | Department of Occupational & Environmental Health, College of Public Health, University of Oklahoma Health Sciences Center
Dear Readers,

This is Changjie Cai, the corresponding author of this letter. Please note that it would be great if your decontamination methods would not affect the filtration efficiencies of the N95 respirators. Many thanks for your great contributions of addressing the shortage of supplies during the COVID-19 pandemic! Please share your methods with people who are working on the front-lines! This paper is asking people to think twice before the decontamination, also recommend measuring the filtration efficiency by aerosol size, instead of the total filtration efficiency (I will talk about the reasons below). There are many potential factors,
which could affect the testing results, including the concentration, relative humidity, dwell time, mask incubation time, RH, temperature, testing aerosol size, measurement devices, etc. I am sorry that you could not find enough details from this research letter due to the word limits. We are urgently constructing our website, which would show all detailed experimental setup. We will also share the results of testing the filtration efficiency by aerosol size for untreated KN95 from various manufacturers to the public for free as well.

As you might notice from the letter, there are many differences between our testing method and NIOSH filtration efficiency test method (procedure No. TEB-APR-STP-0059). For example, we incubated the mask at temperature of 38 °C and 100% relative humidity. If you are using NIOSH method, the RH is 80% I think. In order to better protect our health personnel, we were testing the worst scenario, and we feel this might be more real, since our exhalation RH is actually saturated (~100%).

The testing aerosol size is actually my big concern. The current NIOSH filtration efficiency test method (procedure No. TEB-APR-STP-0059) might overestimate the mask capability. The NIOSH recommended testing aerosol with count median diameter of 75 nm ± 20 nm and geometric standard deviation ≤1.86, the size of which might be too small. We tested various KN95 from over 20 manufacturers. Here is an example. One unqualified KN95 respirator (with the filtration efficiency of 72%±3% for ≥300 nm sodium chloride aerosol) still passed the test with a measured overall filtration efficiency of 98%±0.5%. We published the draft at a preprint server: https://www.medrxiv.org/content/10.1101/2020.05.14.20102327v2
The results for the above failure might be that the most penetrating particle size shifted from 30 nm – 300 nm to 250 nm – 500 nm. Therefore, we recommend testing the filtration efficiency by aerosol size instead of the overall filtration efficiency.

I am an aerosol scientist, and I did not notice those issues until I start testing the masks for the hospitals during this pandemic. Hopefully, those issues could catch people’s attentions in the future.

Please also note that our studies only tested the filtration efficiency of the mask materials, not the fit test. FIT TEST is also extremely important. For example, the surgical face masks have much lower fit quality compared to N95 grade respirators.

Please feel free to shoot me an email (changjie-cai@ouhsc.edu) or leave your comments here if you have any question. Please stay safe and health!

In peace,
Changjie

Changjie Cai, Ph.D., Assistant Professor
Department of Occupational and Environmental Health
Hudson College of Public Health, University of Oklahoma
O: (405)271-2070 x 46774 | F: (405)271-1971
CONFLICT OF INTEREST: None Reported
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Feasibility of Sterilization of Masks in Real Life Setting
Amit Sandhu, Ph.D. | Advanced Pediatric Center, Postgraduate Institute of Medical Education and Research, Chandigarh, INDIA
We read this study with interest. Although it is a very informative study but we perceive that it will more effective if they added some other prospects related to masks.

An important aspect of coronavirus or any other infectious agent is its availability on a specific surface. A recent study evaluated the stability of SARS-CoV-1 and SARS-CoV-2 on various surfaces and estimated their decay rate. They reported the stability of SARS-CoV-2 on plastic and stainless steel up to 72 hours after application to these surfaces. On copper and cardboard, it is 8 hours for SARS-CoV-1 for each and 4
hrs and 24 hrs for SARS-CoV-2 respectively (1). In real life, it will also depend on viral load in the upper respiratory tract and the possibility of shedding and transmission by asymptomatic persons. So assuming, if masks reached disinfection center after the given time period then it is a waste of sources. Moreover, it is also not feasible to track the record of each mask. Furthermore, the retention of any part of that chemical may also lead to toxic or allergic reactions.

Moreover, as per Cai et al, plasma vapor hydrogen peroxide (H2O2) treatment retained 95% efficiency in N95 and KN95 mask but there is a significant reduction in efficiency of surgical mask; however, they did not mention the effect of these chemicals on overall shape and fitting of masks. Elastic materials which are used to hold the mask and metal strip to fasten it to the face also play an important role. If after treatment these parts are disturbed (deformation of elasticity or accumulation of humidity), then there is no use of that mask (2). A loosely or improper fitted mask may again increase the incidence of disease. Hence proper technology and resources will also be required for the decontamination process. Furthermore, peoples are using homemade or non-certified masks these days due to obvious economic reasons; hence efficiency and sterilization studies on these are priorities.

Alongside this comparison of chemical methods with other physical methods like sunlight, steam, UV rays, etc needs to be explored in terms of efficacy, feasibility, and economic aspects, as a sustainable method will be much needed on a large scale in the near future.

References:
1. Van Doremalen N, Bushmaker T, Morris DH, et al. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. New England Journal of Medicine. 2020;382(16):1564-1567.
2. Carlos Rubio-Romero J, Del Carmen Pardo-Ferreira M, Antonio Torrecilla García J, Calero-Castro S. Disposable masks: Disinfection and sterilization for reuse, and non-certified manufacturing, in the face of shortages during the COVID-19 pandemic. Saf Sci. 2020;129(104830):104830.
CONFLICT OF INTEREST: None Reported
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Important Correction of this Paper!
Changjie Cai, Ph.D. | Department of Occupational & Environmental Health, College of Public Health, University of Oklahoma Health Sciences Center
Dear Readers,

Again, this is Changjie Cai, the corresponding author of this letter. We found an error need to be corrected that the disinfectant the hospitals used for sterilization is “Vital Oxide” instead of “Chlorine Dioxide.” A formal correction is in progress to correct the “Chlorine Dioxide” and “ClO2” in the manuscript to “Vital Oxide.”

“Chlorine Dioxide” is the effective ingredient in the “Vital Oxide” of killing viruses and bacterial, but it is NOT the ONLY ingredient. Our lab has been conducting mask filtration efficiency tests of various masks for the OU hospitals due to the COVID-19 pandemic
and short of mask supplies. The error occurred due to the miscommunication.

I sincerely apologize for this.

Please feel free to shoot me an email (changjie-cai@ouhsc.edu) or leave your comments here if you have any question. Please stay safe and health,
In peace,

Changjie Cai, Ph.D., Assistant Professor
Department of Occupational and Environmental Health
Hudson College of Public Health, University of Oklahoma
O: (405)271-2070 x 46774 | F: (405)271-1971
CONFLICT OF INTEREST: None Reported
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Clarifications
Daniela Schneider, PhD Student | Federal University of Rio Grande do Sul - UFRGS, Porto Alegre, RS, Brazil
Can the authors clarify the following:

- Control group size

- Information about the time and temperature of the sterilization cycles used

- What sterilization equipment, model and brand used in the study?
CONFLICT OF INTEREST: None Reported
Research Letter
Occupational Health
June 15, 2020

Effects of Sterilization With Hydrogen Peroxide and Chlorine Dioxide Solution on the Filtration Efficiency of N95, KN95, and Surgical Face Masks

Author Affiliations
  • 1Department of Occupational and Environmental Health, University of Oklahoma Health Sciences Center, University of Oklahoma, Oklahoma City
JAMA Netw Open. 2020;3(6):e2012099. doi:10.1001/jamanetworkopen.2020.12099
Introduction

Owing to the coronavirus disease 2019 pandemic, there is a global shortage of masks needed to protect health care personnel.1,2 The US Centers for Disease Control and Prevention has suggested the potential reuse of disposable respirators to conserve available supplies.3 A study by Viscusi et al4 evaluated various sterilization methods for reuse of N95 masks. Although surgical masks should not be used as a substitute for N95s owing to lower fit quality,5 a randomized clinical trail by Radonovich et al6 found that there was no significant difference in the incidence of laboratory-confirmed influenza among health care personnel who used N95s vs surgical face masks. The Centers for Disease Control and Prevention listed KN95 masks (the Chinese version of the N95) as suitable alternatives to N95s when N95s are not available. However, to our knowledge, there are no studies regarding the effects of sterilization on the filtration efficiencies of KN95s or surgical face masks. The goal of this quality improvement study was to test the feasibility of reusing KN95s and surgical masks.

Methods

The University of Oklahoma institutional review board determined that this study was not human research and was exempt from informed consent. This study is reported following the Standards for Quality Improvement Reporting Excellence (SQUIRE) reporting guideline. This study was conducted from March 25 to April 7, 2020.

We compared sterilization by plasma vapor hydrogen peroxide (H2O2) and a chlorine dioxide solution, Vital Oxide, on the filtration efficiencies of 3 types of masks, N95s (model 1860; 3M), KN95s (Civilian Antivirus; Qingdao Sophti Health Technology), and surgical face masks (model 1541; Dukal). Experiments were conducted using the test chamber illustrated in eFigure 1 in the Supplement. A stable salt aerosol (eFigure 2 in the Supplement) was generated using a 3-jet Collison nebulizer (CH Technologies) and 2% sodium chloride solution in accordance with National Institute of Occupational Safety and Health procedure No. TEB-APR-STP-0059. A scanning mobility particle sizer (model 3936; TSI) was used to measure the particle number concentration from 16.8 nm to 514 nm. All masks were preconditioned in an incubator at 38 °C and 100% relative humidity for 12 hours. For each mask, 5 samples were tested with 4 upstream measurements and 4 downstream measurements. Acceptable pressure drop was defined as less than 35 mm or 1.38 inch water for inhalation. We calculated the mean and SD of filtration efficiency and pressure drop for each type mask.

Results

The effects of sterilization on overall filtration efficiency and pressure drop are summarized in Figure 1. The mean (SD) filtration efficiencies of untreated masks were 97.3% (0.4%) for N95s, 96.7% (1.0%) for KN95s, and 95.1% (1.6%) for surgical face masks. After H2O2 sterilization, the filtration efficiencies were 96.6% (1.0%) for N95s, 97.1% (2.4%) for KN95s, and 91.6% (1.0%) for surgical face masks. The N95s and KN95s retained at least 95% efficiency, but the surgical face mask’s efficiency was reduced. After sterilization with the chlorine dioxide solution, the filtration efficiencies were 95.1% (1.6%) for N95s, 76.2% (2.7%) for KN95s, and 77.9% (3.4%) for surgical face masks. The H2O2 treatment showed a small effect on the overall filtration efficiency of the tested masks, but the chlorine dioxide solution treatment showed marked reduction in the overall filtration efficiency of the KN95s and surgical face masks. All pressure drop changes were within the acceptable range.

The effects of sterilization on filtration efficiency by aerosol size are presented in Figure 2. For all untreated masks, the filtration efficiencies by size were more than 95%. For N95s after sterilization with the chlorine dioxide solution, the mean (SD) filtration efficiency for particles of approximately 300 nm decreased to approximately 86.2% (6.8%), although the overall filtration efficiency was retained at approximately 95%. Therefore, caution should be exercised when using this mask under this condition. The mean (SD) filtration efficiencies decreased to 40.8% (5.9%) for KN95s and 47.1% (14.4%) for surgical face masks for particles of approximately 300 nm.

Discussion

This quality improvement study found that the sterilization processes had different effects on the filtration efficiencies of different masks. Sterilization with H2O2 had fewer negative effects than the chlorine dioxide solution. In addition to considering the overall filtration efficiency, the filtration efficiency for particles similar to infectious agents should be considered. This study has some limitations, including the small variety of mask manufacturers, small sample sizes for each mask and condition, and only 2 sterilization techniques evaluated. In addition, this study only compared the filtration efficiency after 1 sterilization cycle; however, filter material may degrade further after multiple cycles, which should also be investigated. To better protect health care personnel in hospitals, we recommend measuring the respirator’s filtration efficiency by aerosol size instead of only measuring the overall filtration efficiency.

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Article Information

Accepted for Publication: May 19, 2020.

Published: June 15, 2020. doi:10.1001/jamanetworkopen.2020.12099

Correction: This article was corrected on August 14, 2020, to clarify that the chlorine dioxide solution used was Vital Oxide.

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2020 Cai C et al. JAMA Network Open.

Corresponding Author: Changjie Cai, PhD, Department of Occupational and Environmental Health, University of Oklahoma Health Sciences Center, University of Oklahoma, 801 NE 13th St, Room 431, Oklahoma City, OK 73104 (changjie-cai@ouhsc.edu).

Author Contributions: Drs Cai and Floyd had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Both authors.

Acquisition, analysis, or interpretation of data: Both authors.

Drafting of the manuscript: Cai.

Critical revision of the manuscript for important intellectual content: Both authors.

Statistical analysis: Cai.

Obtained funding: Both authors.

Administrative, technical, or material support: Both authors.

Supervision: Both authors.

Conflict of Interest Disclosures: None reported.

Funding/Support: This study was supported by the Oklahoma State Department of Health to establish this testing program; the supply chain logistics group at the University of Oklahoma Medicine, which provided the respirators and sterilization treatments; and the University of Oklahoma Health Sciences Center VPR’s office through a COVID-19 Rapid Response pilot grant.

Role of the Funder/Sponsor: The funders were involved in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, and approval of the manuscript; and decision to submit the manuscript for publication.

References
1.
Wu  HL, Huang  J, Zhang  CJP, He  Z, Ming  WK.  Facemask shortage and the novel coronavirus disease (COVID-19) outbreak: reflections on public health measures.   EClinicalMedicine. April 3, 2020;100329. doi:10.1016/j.eclinm.2020.100329PubMedGoogle Scholar
2.
Feng  S, Shen  C, Xia  N, Song  W, Fan  M, Cowling  BJ.  Rational use of face masks in the COVID-19 pandemic.   Lancet Respir Med. 2020;8(5):434-436. doi:10.1016/S2213-2600(20)30134-XPubMedGoogle ScholarCrossref
3.
Centers for Disease Control and Prevention. Recommended guidance for extended use and limited reuse of N95 filtering facepiece respirators in healthcare settings. Accessed May 21, 2020. https://www.cdc.gov/niosh/topics/hcwcontrols/recommendedguidanceextuse.html
4.
Viscusi  DJ, Bergman  MS, Eimer  BC, Shaffer  RE.  Evaluation of five decontamination methods for filtering facepiece respirators.   Ann Occup Hyg. 2009;53(8):815-827.PubMedGoogle Scholar
5.
Derrick  JL, Gomersall  CD.  Protecting healthcare staff from severe acute respiratory syndrome: filtration capacity of multiple surgical masks.   J Hosp Infect. 2005;59(4):365-368. doi:10.1016/j.jhin.2004.10.013PubMedGoogle ScholarCrossref
6.
Radonovich  LJ  Jr, Simberkoff  MS, Bessesen  MT,  et al; ResPECT investigators.  N95 respirators vs medical masks for preventing influenza among health care personnel: a randomized clinical trial.   JAMA. 2019;322(9):824-833. doi:10.1001/jama.2019.11645PubMedGoogle ScholarCrossref
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